Abstract

Background

Trigeminal proprioception related to rodent macrovibrissae movements is believed to
involve skin receptors on the whisker pad because pad muscles operate without muscle
spindles. This study was aimed to investigate in rats whether the trigeminal mesencephalic
nucleus (TMnu), which provides proprioceptive feedback for chewing muscles, may be
also involved in whisker pad proprioception.

Methods

Two retrograde tracers, Dil and True Blue Chloride, were injected into the mystacial
pad and the masseter muscle on the same side of deeply anesthetized rats to label
the respective projecting sensory neurons. This double-labeling technique was used
to assess the co-innervation of both structures by the trigeminal mesencephalic nucleus
(TMnu).

In a separate group of anesthetized animals, the spontaneous electrical activities
of TMnu neurons were analyzed by extracellular recordings during spontaneous movements
of the macrovibrissae. Mesencephalic neurons (TMne) were previously identified by
their responses to masseter muscle stretching. Changes in TMne spontaneous electrical
activities, analyzed under baseline conditions and during whisking movements, were
statistically evaluated using Student's t-test for paired observations.

Results

Neuroanatomical experiments revealed different subpopulations of trigeminal mesencephalic
neurons: i) those innervating the neuromuscular spindles of the masseter muscle, ii)
those innervating the mystacial pad, and iii) those innervating both structures. Extracellular
recordings made during spontaneous movements of the macrovibrisae showed that whisking
neurons similar to those observed in the trigeminal ganglion were located in the TMnu.
These neurons had different patterns of activation, which were dependent on the type
of spontaneous macrovibrissae movement. In particular, their spiking activity tonically
increased during fan-like movements of the vibrissae and showed phasic bursting during
rhythmic whisking. Furthermore, the same neurons may also respond to masseter muscle
stretch.

Conclusions

results strongly support the hypothesis that the TMnu also contains first-order neurons
specialized for relaying spatial information related to whisker movement and location
to trigeminal-cortical pathways. In fact, the TMnu projects to second-order trigeminal
neurons, thus allowing the rat brain to deduce higher-order information regarding
executed movements of the vibrissae by combining touch information carried by trigeminal
ganglion neurons with proprioceptive information carried by mesencephalic neurons.